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A pilot study to understand tooth replacement in near-harvest farmed saltwater crocodiles (Crocodylus porosus): Implications for blemish induction
Abstract
Saltwater crocodiles (Crocodylus porosus) are farmed in Australia primarily for their belly skin. The desirability and ultimately the value of each skin depends on the extent and location of various industry-defined defects. Anecdotal observations suggest that conspecific interactions are the main contributors with the protrusive 4th dentary teeth (i.e. eye teeth) the most likely cause. It is well known that crocodilians undergo continual tooth replacement, yet no study has investigated tooth replacement rates or tooth growth dynamics in juvenile saltwater crocodiles. In this pilot study, we repeatedly measured eye tooth crown height and observed eye tooth replacement in individually-housed juvenile saltwater crocodiles (n = 98) accounting for 290 individual teeth. The majority of teeth were replaced every three to six months (n = 172) but nine teeth were not replaced over the 15-month study period. After a tooth was lost, the need to replace it quickly was evidenced by a faster tooth growth rate in the first three months (11.07 ± 0.17 mm) but subsequently slowed to a model-adjusted asymptote of 14.03 ± 0.27 mm (p <.001). Interestingly, teeth on the left side of the mandible were, on average, 0.43 ± 0.16 mm shorter than those on the right (p <.001) and, although just outside 5% significance, were replaced 1.20 times as often. Together this is suggestive that crocodiles may preference food capture with the left-hand side of their mouth but requires more structured behavioural observations to confirm. Unusually, the eye-teeth of eight crocodiles did not protrude, which is a normal characteristic of crocodiles compared to alligators, but instead were observed to be growing into the interior of the mouth. This study begins to provide some context to tooth biology when preemptive solutions to tooth-induced blemishes are being sought.
... Crocodylian dentition has been of key interest in the study of reptilian biology because crocodiles are equipped with a highly specialised con tinuous tooth replacement (Poole, 1961;Finger et al., 2019;Whitlock & Richman, 2013). This process has resulted in large, empty pulp chambers comprising most of the tooth's internal structure, with a cap of dentine filling most of the small crown, and a relatively thin layer of enamel coating the entire tooth, including the root. ...
... Both modern and fossil crocodylian tooth structure and function have been studied, including experimental bio mechanics of biting force, tooth replacement questions, and dentine incremental lines in alligatorids (e.g. Enax et al., 2013;Poole, 1961;Finger et al., 2019;Dauphin & Williams, 2008;Kieser et al., 1993;Szewczyk & Stachewicz, 2020;Kundanati et al., 2019;Sato et al., 1990;Mishima et al., 2003), but limited dental histology data exist in other members of the order. Crocodile dental enamel is particularly thin (relative to dentine in other reptiles), reportedly in the order of 100-200 μm in C. porosus (Enax et al., 2013). ...
... According to the studies conducted by Kear et al. (2017) and Maxwell et al. (2011aMaxwell et al. ( ,b, 2012, the mineralization time for the teeth was estimated to be at most 2 to 3 years for plesiosaurs and approximately 1 year for ichthyosaurs. Although there is currently no available information regarding the tooth renewal time of Metriorhynchidae, it can be assumed that it was comparable to that of extant crocodylomorphs, which is approximately 3 to 15 months (Erickson 1996;Finger et al. 2019). In Ichthyosauria and Plesiosauria, bones underwent regular remodeling throughout life, as evidenced by studies conducted by Kolb et al. (2011), Delsett and, Houssaye et al. (2014), andO'Keefe et al. (2019). ...
Ichthyosauria, Plesiosauria, and Metriorhynchidae were apex predators in Mesozoic oceanic trophic networks. Previous stable oxygen isotope studies suggested that several taxa belonging to these groups were endothermic and that some of them were homeothermic organisms. However, these conclusions remain contentious owing to the associated uncertainties regarding the δ ¹⁸ O value and oxygen isotope fractionation relative to environmental seawater. Here, we present new bioapatite phosphate δ ¹⁸ O values (δ ¹⁸ O p ) of Ichthyosauria, Plesiosauria, and Metriorhynchidae (Middle Jurassic to Early Cretaceous) recovered from mid- to high paleolatitudes to better constrain their thermophysiology and investigate the presence of regional heterothermies. The intraskeletal δ ¹⁸ O p variability failed to reveal distinct heterothermic patterns within any of the specimens, indicating either intrabody temperature homogeneity or an overriding diagenetic overprint of the original biological δ ¹⁸ O p bone record. Body temperature estimates have been reassessed from new and published δ ¹⁸ O p values of well-preserved isolated teeth, recently revised Mesozoic latitudinal δ ¹⁸ O oceanic gradients, and ¹⁸ O-enrichment factors of fully aquatic air-breathing vertebrates. Our results confirm that Ichthyosauria were homeothermic endotherms (31°C to 41°C), while Plesiosauria were likely poikilothermic endotherms (27°C to 34°C). The new body temperature estimates of the Metriorhynchidae (25°C to 32°C) closely follow ambient temperatures and point to poikilothermic strategy with no or little endothermic ability. These results improve our understanding of Mesozoic marine reptile thermoregulation and indicate that due to their limited body temperature variations, the δ ¹⁸ O p values from Ichthyosauria fossil remains could be used as valuable archives of Mesozoic oceans δ ¹⁸ O sw values that may help improve paleoenvironmental and paleoclimatic reconstructions.
... The underlying principle for conservation and diversity of teeth is both ascribed to natural evolution for the targeted functions. For example, whereas most mammals are diphyodont-that is, they replace teeth only twice-most other vertebrates are polyphyodont, continuously replacing worn teeth throughout the lifetime [22][23][24]. This difference in the regeneration ability may indicate the different natural design criteria for human teeth and shark teeth. ...
Although the evolution of tooth structure seems highly conserved, remarkable diversity exists among species due to different living environments and survival requirements. Along with the conservation, this diversity of evolution allows for the optimized structures and functions of teeth under various service conditions, providing valuable resources for the rational design of biomimetic materials. In this review, we survey the current knowledge about teeth from representative mammals and aquatic animals, including human teeth, herbivore and carnivore teeth, shark teeth, calcite teeth in sea urchins, magnetite teeth in chitons, and transparent teeth in dragonfish, to name a few. The highlight of tooth diversity in terms of compositions, structures, properties, and functions may stimulate further efforts in the synthesis of tooth-inspired materials with enhanced mechanical performance and broader property sets. The state-of-the-art syntheses of enamel mimetics and their properties are briefly covered. We envision that future development in this field will need to take the advantage of both conservation and diversity of teeth. Our own view on the opportunities and key challenges in this pathway is presented with a focus on the hierarchical and gradient structures, multifunctional design, and precise and scalable synthesis.
... Assumption 1 forms the basis for using a subsection of a transect to derive a mean VEIW for a tooth (Erickson, 1992(Erickson, , 1996a(Erickson, , 1996bGren, 2011;Gren & Lindgren, 2013;Erickson et al., 2017;Kear et al., 2017;Ricart et al., 2019;, but contrasts with a competing hypothesis that teeth have different growth rates during their formation, which would result in wider VEIWs depending on distance from the pulp cavity (Y-H. Wu, 2018, personal communication, Lawson, Wake & Beck, 1971Hanai & Tsuihiji, 2018;Finger, Thomson & Isberg, 2019), as well as with observations of flexible replacement rates coupled with metabolic activity (often seasonally influenced) in extant reptiles (Cooper (1966) in Anguis fragilis, Delgado, Davit-Beal & Sire (2003) in Chalcides sexlineatus and Chalcides viridanus) and mammals (Klevezal, 1996: 66f). Assumption 2 forms the basis for the use of transverse sections to derive tooth formation times (Sereno et al., 2007;Gren, 2011;Gren & Lindgren, 2013;Kear et al., 2017;Ricart et al., 2019). ...
Dietary habits in extinct species cannot be directly observed; thus, in the absence of extraordinary evidence, they must be reconstructed with a combination of morphological proxies. Such proxies often include information on dental organization and function such as tooth formation time and tooth replacement rate. In extinct organisms, tooth formation times and tooth replacement rate are calculated, in part via extrapolation of the space between incremental lines in dental tissues representing daily growth (von Ebner Line Increment Width; VEIW). However, to date, little work has been conducted testing assumptions about the primary data underpinning these calculations, specifically, the potential impact of differential sampling and data extrapolation protocols. To address this, we tested a variety of intradental, intramandibular, and ontogentic sampling effects on calculations of mean VEIW, tooth formation times, and replacement rates using histological sections and CT reconstructions of a growth series of three specimens of the extant archosaurian Alligator mississippiensis. We find transect position within the tooth and transect orientation with respect to von Ebner lines to have the greatest impact on calculations of mean VEIW—a maximum number of VEIW measurements should be made as near to the central axis (CA) as possible. Measuring in regions away from the central axis can reduce mean VEIW by up to 36%, causing inflated calculations of tooth formation time. We find little demonstrable impact to calculations of mean VEIW from the practice of subsampling along a transect, or from using mean VEIW derived from one portion of the dentition to extrapolate for other regions of the dentition. Subsampling along transects contributes only minor variations in mean VEIW (
Synopsis
Reptiles with continuous tooth replacement, or polyphyodonty, replace their teeth in predictable, well-timed waves in alternating tooth positions around the mouth. This process is thought to occur irrespective of tooth wear or breakage. In this study, we aimed to determine if damage to teeth and premature tooth extraction affects tooth replacement timing long-term in juvenile green iguanas (Iguana iguana). First, we examined normal tooth development histologically using a BrdU pulse-chase analysis to detect label-retaining cells in replacement teeth and dental tissues. Next, we performed tooth extraction experiments for characterization of dental tissues after functional tooth (FT) extraction, including proliferation and β-Catenin expression, for up to 12 weeks. We then compared these results to a newly analyzed historical dataset of X-rays collected up to 7 months after FT damage and extraction in the green iguana. Results show that proliferation in the dental and successional lamina (SL) does not change after extraction of the FT, and proliferation occurs in the SL only when a tooth differentiates. Damage to an FT crown does not affect the timing of the tooth replacement cycle, however, complete extraction shifts the replacement cycle ahead by 4 weeks by removing the need for resorption of the FT. These results suggest that traumatic FT loss affects the timing of the replacement cycle at that one position, which may have implications for tooth replacement patterning around the entire mouth.
American alligators Alligator
mississippiensis undergo major transformations in morphology and ecology during development. These include several thousand-fold changes in body mass, modified snout and dental proportions, and shifts in diet from small, delicate foodstuffs to the inclusion of increasingly larger, more robust prey. How these changes in anatomical form contribute to actual physical performance and niche use is largely unknown. In the present study, bite-force measurements for 41 specimens of A.
mississipiensis, were made throughout ontogeny (hatchling–older adults) using a series of precision force transducers. How this performance indicator scaled with respect to cranial and whole-body measurements was determined. Bite-force production throughout development was contrasted with ontogenetic changes in trophic ecology. The influences of this performance measure on these changes were then analysed. The results showed a 800-fold range (12–9452 N) of bite forces with values positively correlating with increases in body size. Scaling of biting forces through ontogeny showed positive allometry with respect to body mass, head length, jaw length, snout–vent length and total length. These patterns may be attributable to allometric growth of individual skeletal elements (and associated musculature), and/or progressive fusion and ossification of skull and jawbones during development. The overall pattern of force increase throughout ontogeny did not vary in association with major shifts in diet. Notably, the bite-force values for adult A.
mississippiensis are the highest measured for any living animal and represent the first measures for a large crocodilian. Additionally, these data provide the first documentation of how bite force changes during ontogeny in a reptile. By bridging the rich morphological and ecological databases for these animals, this study opens the door to a comprehensive understanding of feeding in A.
mississippiensis. Furthermore, it provides groundwork for standardized comparative studies of feeding among crocodilian, reptilian, or other gnathostome vertebrates.
The foods of wild juvenile saltwater crocodiles (Crocodylus porosus) are described, and rates of feeding, nutrient intake and growth are quantified. The size of prey eaten is strongly bimodal: large numbers of small prey (mainly crustaceans) and small numbers of large prey (mainly rats). The nutrient intake levels reflect size related changes in diet (more larger prey in larger crocodiles). The average juvenile diet is characterized by 70-71% water, low fat levels (3.0-4.5%), high protein content (12.7-14.7%), and calcium:phosphorus ratios which decline from 7:1 in animals 300-599 mm total length (TL), to 2:1 in animals 900-1200 mm TL. A mean food conversion rate (wet weight to wet weight) of 82.4% is derived, which is appreciably higher than results obtained from captive crocodilians (17-40%). To maintain similar growth rates, a wild juvenile C. porosus of 682 mm TL requires food equivalent to 4% of its body weight per week, whereas captive counterparts require four times that amount. The physiological mechanisms associated with digestion and assimilation may not function as efficiently when the stomach is repeatedly filled to capacity, as occurs in captivity.
Interspecific adult bite forces for all extant crocodylian species are now known. However, how bite forces scale during ontogeny across the clade has yet to be studied. Here we test the hypotheses that extant crocodylians share positively allometric and statistically comparable developmental scaling coefficients for maximal bite-force capacity relative to body size. To do this, we measured bite forces in the Australian freshwater crocodile Crocodylus johnsoni and the Saltwater crocodile C. porosus, and determined how performance changed during ontogeny. We statistically compared these results with those for the American alligator Alligator mississippiensis using 95% prediction intervals and interpreted our findings in a phylogenetic context. We found no observable taxon-specific shifts in the intraspecific scaling of biomechanical performance. Instead, all bite-force values in our crocodylid dataset fell within the bounds of the A. mississippiensis 95% prediction intervals, suggesting similar bite-force capacity when same-sized individuals are compared. This holds true regardless of differences in developmental stage, potential adult body size, rostro-dental form, bone mineralization, cranial suturing, dietary differences or phylogenetic relatedness. These findings suggest that intraspecific bite-force scaling for crocodylians with feeding ecologies comparable with those of extant forms has likely remained evolutionarily static during their diversification.
Minimising stress in farmed crocodiles is not only important for improving animal welfare, but may also improve skin blemish healing and infection resistance, which influence the quality of the final skin product. Forty near-harvest size saltwater crocodiles (1.6-1.8 m TL) from two Australian farms were sampled to evaluate the effect of different pen types (communal pens n=20; individual pens n=20) on stress as indicated by plasma corticosterone. Blood samples were taken within three minutes of immobilisation and analysed using a commercial enzyme immunoassay kit. There was no relationship with animal size (P=0.16), between farms (P=0.86), pen types (P=0.69), communal pens between farms (P=0.28) or individual pens between farms (P=0.24). Based on corticosterone levels, it appears that individual pens do not cause significantly more stress on harvest-size animals than communal pens. Individual pens meet their design specifications by achieving comparable healing rates of belly skin blemishes as communal pens without compromising animal welfare and minimising the possibility of new blemishes.
A review of crocodylian phylogeny reveals a more complex history than might have been anticipated from a direct reading of the fossil record without consideration of phylogenetic relationships. The three main extant crocodylian lineagesGavialoidea, Alligatoroidea, Crocodyloideaare known from fossils in the Late Cretaceous, and the group is found nearly worldwide during the Cenozoic. Some groups have distributions that are best explained by the crossing of marine barriers during the Tertiary. Early Tertiary crocodylian faunas are phylogenetically composite, and clades tend to be morphologically uniform and geographically widespread. Later in the Tertiary, Old World crocodylian faunas are more endemic. Crocodylian phylogeneticists face numerous challenges, the most important being the phylogenetic relationships and time of divergence of the two living gharials (Gavialis gangeticus and Tomistoma schlegelii), the relationships among living true crocodiles (Crocodylus), and the relationships among caimans.
Reptiles and fish have robust regenerative powers for tooth renewal. However, extant mammals can either renew their teeth one time (diphyodont dentition) or not at all (monophyodont dentition). Humans replace their milk teeth with permanent teeth and then lose their ability for tooth renewal. Here, we study tooth renewal in a crocodilian model, the American alligator, which has well-organized teeth similar to mammals but can still undergo life-long renewal. Each alligator tooth is a complex family unit composed of the functional tooth, successional tooth, and dental lamina. Using multiple mitotic labeling, we map putative stem cells to the distal enlarged bulge of the dental lamina that contains quiescent odontogenic progenitors that can be activated during physiological exfoliation or artificial extraction. Tooth cycle initiation correlates with β-catenin activation and soluble frizzled-related protein 1 disappearance in the bulge. The dermal niche adjacent to the dermal lamina dynamically expresses neural cell adhesion molecule, tenascin-C, and other molecules. Furthermore, in development, asymmetric β-catenin localization leads to the formation of a heterochronous and complex tooth family unit configuration. Understanding how these signaling molecules interact in tooth development in this model may help us to learn how to stimulate growth of adult teeth in mammals.
Saltwater crocodiles (Crocodylus porosus) across three size categories (hatchlings, grower and harvest-size) were repeatedly blood sampled on two farms in the Northern Territory, Australia to determine reference plasma corticosterone (CORT; crocodilian stress hormone) levels. The mean CORT values for hatchlings (<1 year old), growers (1-3 years) and harvest-size individuals (2+ years) were 1.65 ± 0.15 ng/ml, 2.73 ± 0.21 ng/ml and 2.19 ± 0.16 ng/ml, respectively. No inter-farm differences within the hatchling or harvest-size crocodiles were detected, but growers on Farm 2 had significantly lower plasma CORT than those on Farm 1. However, the grower growth rate coefficients were the same across both farms so the repeated blood sampling design most likely contributed to the difference in CORT values rather than any management procedures. Plasma corticosterone levels significantly increased with time of day. Substantial variation in plasma CORT was observed at each sampling which is not unprecedented in the literature but requires further elucidation. Irrespective, as CORT values were generally low, our results suggest that the farming environment and husbandry practices, as implemented under the Australian industry Code of Practice, are effective as baseline animal welfare measures although they should be viewed as a foundation for further welfare research and not considered static.
Between hatching and late adulthood American alligators Alligator mississippiensis show up to 7000-fold increases in body mass. Concurrent with such changes in body size are absolute and relative modifications in rostral proportions, dental form, feeding capacities and dietary preferences. How these major anatomical changes accommodate prey-resource shifts is poorly understood. In this study, we focus on the effects of ontogenetic changes in bite-force capacities and dental form to address how these factors relate to tooth-pressure generation and diet. We derive absolute values of tooth pressure along the crowns of the most prominent teeth (the first documentation of tooth pressures throughout ontogeny and after initial tooth contact for any animal) and show that these pressures increase with positive allometry during ontogeny. In addition, we discuss how American alligator tooth-pressure values explain their capacities for seizure and oral processing of typical prey, and how tooth-pressure changes facilitate developmental niche shifts in this large-bodied taxon.
Juvenile estuarine crocodiles captured insects and crabs at or above the water surface by leaps and lunges powered by the hind limbs and tail. The mouth opened as the head cleared the water; most prey were held by sidesnaps of the jaws. Such prey capture was accurate, deliberate and preceded by stalking. In contrast, submerged prey (e.g. prawns) appeared to be detected mainly by touch and detection was followed by undirected, inaccurate ‘snapping frenzies’ which were usually ineffective. Small prey items were swallowed whole under water. Large dense prey (e.g. crabs) were handled and swallowed on land or in very shallow water; large less dense prey (e.g. cockroaches) were swallowed during vigorous water-treading in deep water, the head being maintained above the water surface.
Young crocodiles ate satiation meals of 9–10% body weight (on a fresh food weight basis) at 30°C, and appetite returned over about 40 h as the stomach emptied. Total gut clearance time for a meal was 4–5 d. Evidence was obtained which demonstrated that young Crocodylus porosus Schneider deliberately eat gastroliths from an early stage. Such gastroliths are retained within the stomach (as were barium/polystyrene spheroids of 1 mm diameter) presumably by the action of the well-developed pyloric sphincter. X-radiographs demonstrated that gastroliths are dispersed throughout the stomach contents after a meal and presumably aid digestion.
Assimilation rates for dry mass (77.5%), energy (85.2%) and protein-N (97.4%) were high in normal juveniles. Animals exhibiting ‘runt syndrome’ showed strong appetite but slow food processing by the gut, together with poor assimilation, especially of protein (35.7%).
The history and replacement of crocodile teeth are described. A new tooth erupts with only a short root which grows downwards into the socket as the pulp cavity in the crown begins to be occluded by the further deposition of dentine. After the root has become fully extended, it is gradually resorbed at its base to make room for an enlarging successional tooth which has been forming on the lingual side of the socket. The successional tooth eventually moves to a position within the partly resorbed functional root and directly under the functional crown. Progressive reduction of the functional root now occurs to accommodate the continuously enlarging successional tooth and, when resorption is largely complete, the functional tooth falls away, allowing the successional tooth, with a short, incomplete root, to take its place. As a result of this successional cycle it is found, within certain limits, that at any given time the form and condition of a functional tooth is related to the size and condition of its successor lying below.
Consideration of various measurements made on a series of twenty-four skulls of different sizes indicates that a regular and continuous replacement of teeth occurs throughout a large part of a crocodile's life. It is estimated that in a crocodile which is thirteen feet long, each tooth is likely to have been replaced forty-five times.
Incremental lines were found in the dentine of Alligator mississippiensis and Caiman crocodilus. Fluorochrome markers indicate that these increments form daily in juvenile alligators. By counting the total number of incremental lines in a functional tooth and subtracting the number in the successive replacement tooth, it is possible to ascertain the replacement rate for the tooth position. Counts done on teeth of mean size for individuals give reasonable estimates of the mean replacement rates for the entire dentition. The tooth replacement rates were monitored for 11 months in juvenile alligators to test this methodology. The hypothesized reduction of tooth replacement rate with ontogeny was supported. © 1996 Wiley-Liss, Inc.
This study compared the stress induced in captive estuarine crocodiles, Crocodylus porosus, by two different handling methods: manual restraint (noosing with ropes) and immobilization by electro-stunning. To stun, a short charge (approx. 6 s) at 110 V was delivered to the back of the necks of C. porosus using a custom-built device, which immobilized the animals for 5-10 min. Immobilized and restrained animals were measured and sexed, and the condition of the skin assessed. Blood samples were taken from some animals immediately after restraint or immobilization. Other animals were returned to their pens to recover for periods of 30 min, 1, 4, 12, 24 or 48 hours after which they were stunned and blood samples taken. Individual animals (mean body length 1.96 m, N=99) were bled only once. Haematocrit and haemoglobin concentrations were measured and plasma samples were analysed for corticosterone, glucose and lactate levels. Following restraint, there were significant increases in haematocrit, haemoglobin, glucose, lactate and corticosterone concentrations in C. porosus. For restrained animals, recovery to baseline levels occurred after approximately 8 hours. The stress response of stunned animals was significantly reduced compared to manually captured and restrained crocodiles. Both groups showed a significant increase in haematocrit, haemoglobin concentration and lactate levels, however the magnitude of change was significantly reduced, and recovery was faster in stunned animals. No increase in either glucose or corticosterone levels occurred with immobilisation. The results imply that immobilization by electro-stunning is much less stressful.
Repeatability and phenotypic correlations were estimated for saltwater crocodile reproductive traits. No pedigree information was available to estimate heritability or genetic correlations, because the majority of breeder animals on farms were wild-caught. Moreover, as the age of the female breeders could not be accounted for, egg-size measurements were used as proxies. The reproductive traits investigated were clutch size (total number of eggs laid), number of viable eggs, number of eggs that produced a live, healthy hatchling, hatchability, average snout-vent length of the hatchlings and time of nesting. A second data set was also created comprising binary data of whether or not the female nested. Repeatability estimates ranged from 0.24 to 0.68 for the measurable traits, with phenotypic correlations ranging from -0.15 to 0.86. Repeatability for whether a female nested or not was 0.58 on the underlying scale. Correlations could not be estimated between the measurement and binary traits because of confounding. These estimates are the first published for crocodilian reproduction traits.
Tracking crocodile skin defects: from farm to product
- C Manolis
- G J Webb
Manolis, C., Webb, G.J., 2011. Tracking crocodile skin defects: from farm to product. In:
Rural Industries Research and Development Corporation. Paper No. 11/012,.
https://www.agrifutures.com.au/wp-content/uploads/publications/11-012.pdf (accessed 17 November 2018).